Abstract
The role of trees, in addition to that of the soil, must be considered in CH4 budget for forests. Although trees can emit CH4 through their stems, there are uncertainties about the main factors that explain inter- and intraspecific variations, which impedes upscaling of measurements from the stem to the ecosystem level. This study aimed to characterize the variability in CH4 emissions (\(F_{{{\text{CH}}_{4} }}\)) from stems between species and individuals, and within individuals. We measured \(F_{{\rm CH}_{4}}\) in situ during the snow-free period in five species in a temperate mountain forest, using individuals of different sizes and chambers at different heights along the stems. One coniferous species emitted almost no CH4, whereas four broadleaved species exhibited high intraspecific variability in \(F_{{\rm CH}_{4}}\) (0–3.7 nmol m−2 s−1). Increasing trends in \(F_{{\rm CH}_{4}}\) with tree diameter were observed for four species. The vertical patterns in \(F_{{\rm CH}_{4}}\) were complex. Seasonal variations in \(F_{{\rm CH}_{4}}\), measured on two trees per species, were well explained by air temperature with apparent temperature sensitivity coefficients (Q10) between 1.2 and 2, which were not related to the antecedent precipitation indices, whether calculated over 7 or 30 days. Potential CH4 production was detected in wood core segments incubated under anoxic conditions in the majority of individual trees of all species. Our results suggest that the CH4 emitted by trunks can originate either from soil or internal sources. Scaling \(F_{{\rm CH}_{4}}\) from trees at the stand level and developing process-based models of \(F_{{\rm CH}_{4}}\) will remain challenging until the sources of variation are better explained.
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Data Availability
The datasets analysed during the current study are available at the Dryad repository (Epron 2022): https://doi.org/10.5061/dryad.hx3ffbggx.
References
Abell CA, Hursh CR. 1931. Positive gas and water pressure in oaks. Science 73:449–449.
Barba J, Bradford MA, Brewer PE, Bruhn D, Covey K, van Haren J, Megonigal JP, Mikkelsen TN, Pangala SR, Pihlatie M, Poulter B, Rivas-Ubach A, Schadt CW, Terazawa K, Warner DL, Zhang Z, Vargas R. 2019. Methane emissions from tree stems: a new frontier in the global carbon cycle. New Phytol 222:18–28.
Barba J, Poyatos R, Capooci M, Vargas R. 2021. Spatiotemporal variability and origin of CO2 and CH4 tree stem fluxes in an upland forest. Global Change Biol 27:4879–4893.
Bates D, Mächler M, Bolker B, Walker S. 2015. Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48.
Bréchet LM, Daniel W, Stahl C, Burban B, Goret J, Salomόn RL, Janssens IA. 2021. Simultaneous tree stem and soil greenhouse gas (CO2, CH4, N2O) flux measurements: a novel design for continuous monitoring towards improving flux estimates and temporal resolution. New Phytol 230:2487–2500.
Carmichael MJ, Bernhardt ES, Bräuer SL, Smith WK. 2014. The role of vegetation in methane flux to the atmosphere: should vegetation be included as a distinct category in the global methane budget? Biogeochemistry 119:1–24.
Covey KR, Megonigal JP. 2019. Methane production and emissions in trees and forests. New Phytol 222:35–51.
Covey KR, Wood SA, Warren RJ, Lee X, Bradford MA. 2012. Elevated methane concentrations in trees of an upland forest. Geophys Res Lett 39:L15705.
Dunfield P, Knowles R, Dumont R, Moore T. 1993. Methane production and consumption in temperate and subarctic peat soils: Response to temperature and pH. Soil Biol Biochem 25:321–326.
Dutaur L, Verchot LV. 2007. A global inventory of the soil CH4 sink. Global Biogeochem Cycles 21:GB4013.
Epron D. 2022. Stem methane emissions and wood methane production. Dryad Dataset. https://doi.org/10.5061/dryad.hx3ffbggx.
Feng H, Guo J, Ma X, Han M, Kneeshaw D, Sun H, Malghani S, Chen H, Wang W. 2022. Methane emissions may be driven by hydrogenotrophic methanogens inhabiting the stem tissues of poplar. New Phytol 233:182–193.
Flanagan LB, Nikkel DJ, Scherloski LM, Tkach RE, Smits KM, Selinger LB, Rood SB. 2021. Multiple processes contribute to methane emission in a riparian cottonwood forest ecosystem. New Phytol 229:1970–1982.
Gauci V, Gowing DJG, Hornibrook ERC, Davis JM, Dise NB. 2010. Woody stem methane emission in mature wetland alder trees. Atmos Environ 44:2157–2160.
Hook DD, Brown CL. 1972. Permeability of the cambium to air in trees adapted to wet habitats. Bot Gaz 133:304–310.
Iguchi H, Sato I, Sakakibara M, Yurimoto H, Sakai Y. 2012. Distribution of methanotrophs in the phyllosphere. Biosci Biotechnol Biochem 76:1580–1583.
Ishihara MI, Suzuki SN, Nakamura M, Enoki T, Fujiwara A, Hiura T, Homma K, Hoshino D, Hoshizaki K, Ida H, Ishida K, Itoh A, Kaneko T, Kubota K, Kuraji K, Kuramoto S, Makita A, Masaki T, Namikawa K, Niiyama K, Noguchi M, Nomiya H, Ohkubo T, Saito S, Sakai T, Sakimoto M, Sakio H, Shibano H, Sugita H, Suzuki M, Takashima A, Tanaka N, Tashiro N, Tokuchi N, Yoshida T, Yoshida Y. 2011. Forest stand structure, composition, and dynamics in 34 sites over Japan. Ecol Res 26:1007–1008.
Ishizuka S, Sakata T, Sawata S, Ikeda S, Sakai H, Takenaka C, Tamai N, Onodera S, Shimizu T, Kan-na K, Tanaka N, Takahashi M. 2009. Methane uptake rates in Japanese forest soils depend on the oxidation ability of topsoil, with a new estimate for global methane uptake in temperate forest. Biogeochemistry 92:281–295.
IUSS Working Group WRB. 2015. World Reference Base for Soil Resources 2014, update 2015. International soil classification system for naming soils and creating legends for soil maps. Roma: FAO
Jeffrey LC, Maher DT, Chiri E, Leung PM, Nauer PA, Arndt SK, Tait DR, Greening C, Johnston SG. 2021a. Bark-dwelling methanotrophic bacteria decrease methane emissions from trees. Nat Commun 12:2127.
Jeffrey LC, Maher DT, Tait DR, Johnston SG. 2020. A small nimble in situ fine-scale flux method for measuring tree stem greenhouse gas emissions and processes (S.N.I.F.F). Ecosystems 23:1676–1689.
Jeffrey LC, Maher DT, Tait DR, Reading MJ, Chiri E, Greening C, Johnston SG. 2021b. Isotopic evidence for axial tree stem methane oxidation within subtropical lowland forests. New Phytol 230:2200–2212.
Jeffrey LC, Reithmaier G, Sippo JZ, Johnston SG, Tait DR, Harada Y, Maher DT. 2019. Are methane emissions from mangrove stems a cryptic carbon loss pathway? Insights from a catastrophic forest mortality. New Phytol 224:146–154.
Koehler MA, Linsley RK. 1951. Predicting the runoff from storm rainfall. Research Paper no. 34. Weather Bureau, US Dept of Commerce, Washington, USA.
Köhn D, Günther A, Schwabe I, Jurasinski G. 2020. Short-lived peaks of stem methane emissions from mature black alder (Alnus glutinosa (L.) Gaertn.)—Irrelevant for ecosystem methane budgets? Plant Environm Interact :pei3.10037.
Lenhart K, Bunge M, Ratering S, Neu TR, Schüttmann I, Greule M, Kammann C, Schnell S, Müller C, Zorn H, Keppler F. 2012. Evidence for methane production by saprotrophic fungi. Nat Commun 3:1046.
Li H-L, Zhang X-M, Deng F-D, Han X-G, Xiao C-W, Han S-J, Wang Z-P. 2020. Microbial methane production is affected by secondary metabolites in the heartwood of living trees in upland forests. Trees 34:243–254.
Machacova K, Bäck J, Vanhatalo A, Halmeenmäki E, Kolari P, Mammarella I, Pumpanen J, Acosta M, Urban O, Pihlatie M. 2016. Pinus sylvestris as a missing source of nitrous oxide and methane in boreal forest. Sci Rep 6:23410.
Machacova K, Borak L, Agyei T, Schindler T, Soosaar K, Mander Ü, Ah-Peng C. 2021. Trees as net sinks for methane (CH4) and nitrous oxide (N2O) in the lowland tropical rain forest on volcanic Réunion Island. New Phytol 229:1983–1994.
Moldaschl E, Kitzler B, Machacova K, Schindler T, Schindlbacher A. 2021. Stem CH4 and N2O fluxes of Fraxinus excelsior and Populus alba trees along a flooding gradient. Plant Soil 461:407–420.
Morrissey LA, Livingston GP. 1992. Methane emissions from Alaska Arctic tundra: an assessment of local spatial variability. J Geophys Res 97:16661.
Mukhin VA, Voronin PYu. 2007. Methane emission during wood fungal decomposition. Doklady Biol Sci 413:159–160.
Mukhin VA, Voronin PYu. 2011. Methane emission from living tree wood. Russ J Plant Physiol 58:344–350.
Nakada R, Fujisawa Y, Hirakawa Y. 1999a. Soft X-ray observation of water distribution in the stem of Cryptomeria japonica D. Don I: general description of water distribution. J Wood Sci 45:188–193.
Nakada R, Fujisawa Y, Hirakawa Y. 1999b. Soft X-ray observation of water distribution in the stem of Cryptomeria japonica D. Don II: types found in wet-area distribution patterns in transverse sections of the stem. J Wood Sci 45:194–199.
Nakada R, Fujisawa Y, Yamashita K, Hirakawa Y. 2003. Changes in water distribution in heartwood along stem axes in Cryptomeria japonica. J Wood Sci 49:107–115.
Nakagawa S, Johnson PCD, Schielzeth H. 2017. The coefficient of determination R 2 and intra-class correlation coefficient from generalized linear mixed-effects models revisited and expanded. J R Soc Interface 14:20170213.
Ngao J, Epron D, Brechet C, Granier A. 2005. Estimating the contribution of leaf litter decomposition to soil CO2 efflux in a beech forest using 13C-depleted litter. Global Change Biol 11:1768–1776.
Obara H, Maejima Y, Kohyama K, Ohkura T, Takata Y. 2015. Outline of the comprehensive soil classification system of japan—first approximation. Jpn Agric Res Q 49:217–226.
Pangala SR, Enrich-Prast A, Basso LS, Peixoto RB, Bastviken D, Hornibrook ERC, Gatti LV, Ribeiro H, Calazans LSB, Sakuragui CM, Bastos WR, Malm O, Gloor E, Miller JB, Gauci V. 2017. Large emissions from floodplain trees close the Amazon methane budget. Nature 552:230–234.
Pangala SR, Hornibrook ERC, Gowing DJ, Gauci V. 2015. The contribution of trees to ecosystem methane emissions in a temperate forested wetland. Global Change Biol 21:2642–2654.
Pangala SR, Moore S, Hornibrook ERC, Gauci V. 2013. Trees are major conduits for methane egress from tropical forested wetlands. New Phytol 197:524–531.
Pitz S, Megonigal JP. 2017. Temperate forest methane sink diminished by tree emissions. New Phytol 214:1432–1439.
Pitz SL, Megonigal JP, Chang C-H, Szlavecz K. 2018. Methane fluxes from tree stems and soils along a habitat gradient. Biogeochemistry 137:307–320.
Plain C, Epron D. 2021. Pulse labelling of deep soil layers in forest with 13CH4: testing a new method for tracing methane in the upper horizons, understorey vegetation and tree stems using laser-based spectrometry. Biogeochemistry 153:215–222.
Plain C, Ndiaye F-K, Bonnaud P, Ranger J, Epron D. 2019. Impact of vegetation on the methane budget of a temperate forest. New Phytol 221:1447–1456.
R Core Team. 2021. R: A language and environment for statistical computing. http://www.R-project.org/
Riley WJ, Subin ZM, Lawrence DM, Swenson SC, Torn MS, Meng L, Mahowald NM, Hess P. 2011. Barriers to predicting changes in global terrestrial methane fluxes: analyses using CLM4Me, a methane biogeochemistry model integrated in CESM. Biogeosciences 8:1925–1953.
Sakabe A, Takahashi K, Azuma W, Itoh M, Tateishi M, Kosugi Y. 2021. Controlling factors of seasonal variation of stem methane emissions from Alnus japonica in a riparian wetland of a temperate forest. J. Geophys Res. Biogeosci. 126:e2021JG006326.
Salomón RL, De Roo L, Bodé S, Boeckx P, Steppe K. 2021. Efflux and assimilation of xylem-transported CO2 in stems and leaves of tree species with different wood anatomy. Plant Cell Environ 44:3494–3508.
Sano Y, Fujikawa S, Fukazawa K. 1995. Detection and features of wetwood in Quercus mongolica var. grosseserrata. Trees 9:261–268.
Sano Y, Fukazawa K. 1990. Observations of moisture distribution in Fraxinus mandshurica var. japonica maxim. and Kalopanax pictus nakai with soft x-ray photography. Res Bull College Exp For 47:367–388.
Saunois M, Stavert AR, Poulter B, Bousquet P, Canadell JG, Jackson RB, Raymond PA, Dlugokencky EJ, Houweling S, Patra PK, Ciais P, Arora VK, Bastviken D, Bergamaschi P, Blake DR, Brailsford G, Bruhwiler L, Carlson KM, Carrol M, Castaldi S, Chandra N, Crevoisier C, Crill PM, Covey K, Curry CL, Etiope G, Frankenberg C, Gedney N, Hegglin MI, Höglund-Isaksson L, Hugelius G, Ishizawa M, Ito A, Janssens-Maenhout G, Jensen KM, Joos F, Kleinen T, Krummel PB, Langenfelds RL, Laruelle GG, Liu L, Machida T, Maksyutov S, McDonald KC, McNorton J, Miller PA, Melton JR, Morino I, Müller J, Murguia-Flores F, Naik V, Niwa Y, Noce S, O’Doherty S, Parker RJ, Peng C, Peng S, Peters GP, Prigent C, Prinn R, Ramonet M, Regnier P, Riley WJ, Rosentreter JA, Segers A, Simpson IJ, Shi H, Smith SJ, Steele LP, Thornton BF, Tian H, Tohjima Y, Tubiello FN, Tsuruta A, Viovy N, Voulgarakis A, Weber TS, van Weele M, van der Werf GR, Weiss RF, Worthy D, Wunch D, Yin Y, Yoshida Y, Zhang W, Zhang Z, Zhao Y, Zheng B, Zhu Q, Zhu Q, Zhuang Q. 2020. The global methane budget 2000–2017. Earth Syst Sci Data 12:1561–1623.
Schindler T, Mander Ü, Machacova K, Espenberg M, Krasnov D, Escuer-Gatius J, Veber G, Pärn J, Soosaar K. 2020. Short-term flooding increases CH4 and N2O emissions from trees in a riparian forest soil-stem continuum. Sci Rep 10:3204.
Schink B, Ward J, Zeikus JG. 1981. Microbiology of wetwood: role of anaerobic bacterial populations in living trees. J Gen Microbiol 123:313–322.
Schwarze FWMR. 2007. Wood decay under the microscope. Fungal Biol Rev 21:133–170.
Segers R. 1998. Methane production and methane consumption: a review of processes underlying wetland methane fluxes. Biogeochemistry 41:23–51.
Sidle RC, Tsuboyama Y, Noguchi S, Hosoda I, Fujieda M, Shimizu T. 2000. Stormflow generation in steep forested headwaters: a linked hydrogeomorphic paradigm. Hydrol Process 14:17.
Sjögersten S, Siegenthaler A, Lopez OR, Aplin P, Turner B, Gauci V. 2020. Methane emissions from tree stems in neotropical peatlands. New Phytol 225:769–781.
Smith KA, Dobbie KE, Ball BC, Bakken LR, Sitaula BK, Hansen S, Brumme R, Borken W, Christensen S, Priemé A, Fowler D, Macdonald JA, Skiba U, Klemedtsson L, Kasimir-Klemedtsson A, Degórska A, Orlanski P. 2000. Oxidation of atmospheric methane in Northern European soils, comparison with other ecosystems, and uncertainties in the global terrestrial sink. Glob Change Biol 6:791–803.
Sorz J, Hietz P. 2006. Gas diffusion through wood: implications for oxygen supply. Trees 20:34–41.
Stoffel MA, Nakagawa S, Schielzeth H. 2021. partR2: partitioning R2 in generalized linear mixed models. PeerJ 9:e11414.
Stutz SS, Anderson J. 2021. Inside out: Measuring the effect of wood anatomy on the efflux and assimilation of xylem-transported CO2. Plant Cell Environ 44:3490–3493.
Takahashi K, Kosugi Y, Kanazawa A, Sakabe A. 2012. Automated closed-chamber measurements of methane fluxes from intact leaves and trunk of Japanese cypress. Atmos Environ 51:329–332.
Tate KR. 2015. Soil methane oxidation and land-use change—from process to mitigation. Soil Biol Biochem 80:260–272.
Terazawa K, Ishizuka S, Sakata T, Yamada K, Takahashi M. 2007. Methane emissions from stems of Fraxinus mandshurica var. japonica trees in a floodplain forest. Soil Biol Biochem 39:2689–2692.
Terazawa K, Tokida T, Sakata T, Yamada K, Ishizuka S. 2021. Seasonal and weather-related controls on methane emissions from the stems of mature trees in a cool-temperate forested wetland. Biogeochemistry 156:211–230.
Terazawa K, Yamada K, Ohno Y, Sakata T, Ishizuka S. 2015. Spatial and temporal variability in methane emissions from tree stems of Fraxinus mandshurica in a cool-temperate floodplain forest. Biogeochemistry 123:349–362.
Ueda S, Ando M, Kanzaki K. 1993. Forest soil surveys of the Kyoto University Forest in Ashiu II: soil types, grain size, and chemical and physical properties of soils [in Japanese]. Bull Kyoto Univ For 65:94–112.
Wang Z-P, Gu Q, Deng F-D, Huang J-H, Megonigal JP, Yu Q, Lü X-T, Li L-H, Chang S, Zhang Y-H, Feng J-C, Han X-G. 2016. Methane emissions from the trunks of living trees on upland soils. New Phytol 211:429–439.
Wang Z-P, Han S-J, Li H-L, Deng F-D, Zheng Y-H, Liu H-F, Han X-G. 2017. Methane production explained largely by water content in the heartwood of living trees in upland forests: methane in heartwood. J Geophys Res Biogeosci 122:2479–2489.
Wang Z-P, Li H-L, Wu H-H, Han S-J, Huang J-H, Zhang X-M, Han X-G. 2021. Methane concentration in the heartwood of living trees and estimated methane emission on stems in upland forests. Ecosystems 24:1485–1499.
Warner DL, Villarreal S, McWilliams K, Inamdar S, Vargas R. 2017. Carbon dioxide and methane fluxes from tree stems, coarse woody debris, and soils in an upland temperate forest. Ecosystems 20:1205–1216.
Welch B, Gauci V, Sayer EJ. 2019. Tree stem bases are sources of CH4 and N2O in a tropical forest on upland soil during the dry to wet season transition. Glob Change Biol 25:361–372.
Whiting GJ, Chanton JP. 1993. Primary production control of methane emission from wetlands. Nature 364:794–795.
Wittmann C, Pfanz H. 2014. Bark and woody tissue photosynthesis: a means to avoid hypoxia or anoxia in developing stem tissues. Funct Plant Biol 41:940–953.
Yamanaka N, Matumoto A, Oshima Y, Kawanabe S. 1993. Stand structure of Mondori-Dani watershed, Kyoto University forest in Ashiu [in Japanese]. Bull Kyoto Univers For 65:63–76.
Yamao M, Sidle RC, Gomi T, Imaizumi F. 2016. Characteristics of landslides in unwelded pyroclastic flow deposits, southern Kyushu, Japan. Nat Hazards Earth Syst Sci 16:617–627.
Yazawa K, Ishida S. 1965. On the wet-heartwood of some broad-leaved trees grown in Japan. ii: seasonal moisture content of yachidamo and harunire by months. J Fac Agric Hokkaido Univers 54:123–136.
Yip DZ, Veach AM, Yang ZK, Cregger MA, Schadt CW. 2019. Methanogenic Archaea dominate mature heartwood habitats of Eastern Cottonwood (Populus deltoides). New Phytol 222:115–121.
Yu X, Hu X, Peng Y, Wu Z, Zhang Q, Li Z, Shi C, Du K. 2019. Amplicon sequencing reveals different microbial communities in living poplar wetwood and sapwood. Trees 33:851–865.
Zeikus JG, Henning DL. 1975. Methanobacterium arbophilicum sp. nov. An obligate anaerobe isolated from wetwood of living trees. Antonie Van Leeuwenhoek 41:543–552.
Zeikus JG, Ward JC. 1974. Methane formation in living trees: a microbial origin. Science 184:1181–1183.
Acknowledgements
We thank the staff of the Ashiu Forest Research Station of the Field Science Education and Research Centre, Kyoto University, for enabling this research, providing the access to the forest, and sharing tree inventory and climate data. We are grateful to Naoki Okada who help us to identify and find the target trees, Yuri Tanaka for her help during a measurement campaign, and Kenji Takahashi and Ryogo Nakada for helpful discussions and advices. The research was supported by grants from the Kyoto University Foundation and the Research Institute for Sustainable Humanosphere, Kyoto University.
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Epron, D., Mochidome, T., Tanabe, T. et al. Variability in Stem Methane Emissions and Wood Methane Production of Different Tree Species in a Cold Temperate Mountain Forest. Ecosystems 26, 784–799 (2023). https://doi.org/10.1007/s10021-022-00795-0
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DOI: https://doi.org/10.1007/s10021-022-00795-0